Genomes of Plant-Associated Clavicipitaceae

Schardl, Christopher L.; Young, Carolyn; Moore, Neil; Krom, Nick; Dupont, Pierre‐Yves; Pan, Juan; Florea, Simona; Webb, James D.; Jaromczyk, Jolanta; Jaromczyk, Jerzy W.; Cox, Murray P.; Farman, Mark L.

doi:10.1016/b978-0-12-397940-7.00010-0

Cited by 33 publications

(33 citation statements)

References 90 publications

(146 reference statements)

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“…The regions encoding the adenylation (A), thiolation (T), condensation (C), methylation (M), and reductase* (R*) domains are shown within the perA gene map, with numbers indicating whether they are located in the first or second module. Isolates for which perA was subsequently sequenced or for which the perA sequence was already available (16,33,42) are shown in boldface. Low-intensity PCR products indicate the presence of SNPs in the primer target binding sequence.…”

Section: Resultsmentioning

confidence: 99%

Disparate Independent Genetic Events Disrupt the Secondary Metabolism Gene perA in Certain Symbiotic Epichloë Species

Berry

Takach

Schardl

et al. 2015

Appl Environ Microbiol

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Peramine is an insect-feeding deterrent produced by Epichloë species in symbiotic association with C 3 grasses. The perA gene responsible for peramine synthesis encodes a two-module nonribosomal peptide synthetase. Alleles of perA are found in most Epichloë species; however, peramine is not produced by many perA-containing Epichloë isolates. The genetic basis of these peramine-negative chemotypes is often unknown. Using PCR and DNA sequencing, we analyzed the perA genes from 72 Epichloë isolates and identified causative mutations of perA null alleles. We found nonfunctional perA-⌬R* alleles, which contain a transposon-associated deletion of the perA region encoding the C-terminal reductase domain, are widespread within the Epichloë genus and represent a prevalent mutation found in nonhybrid species. Disparate phylogenies of adjacent A2 and T2 domains indicated that the deletion of the reductase domain (R*) likely occurred once and early in the evolution of the genus, and subsequently there have been several recombinations between those domains. A number of novel point, deletion, and insertion mutations responsible for abolishing peramine production in full-length perA alleles were also identified. The regions encoding the first and second adenylation domains (A1 and A2, respectively) were common sites for such mutations. Using this information, a method was developed to predict peramine chemotypes by combining PCR product size polymorphism analysis with sequencing of the perA adenylation domains. Fungal secondary metabolites are a diverse group of important but often nonessential organic compounds with a wide range of properties that are likely to be advantageous for the producing organism or in some cases essential for pathogenicity or developmental stages (1-3). These low-molecular-weight compounds tend to only be produced under certain environmental or growth conditions. The biosynthetic pathways for production of any particular class of secondary metabolites are common to many fungi, but production of a specific secondary metabolite is often unique to a small phylogenetic group of species (4). Epichloë species are fungal endophytes of C 3 grasses that are known to produce several bioactive alkaloids that provide bioprotective properties to the host plant (5). These secondary metabolites include the indolediterpenes, ergot alkaloids, lolines, and peramine ( Fig. 1) (6, 7). The indole-diterpene lolitrem B and ergot alkaloid ergovaline have significant detrimental effects on the health and production of stock animals that graze infected pastures (7,8). The lolines are insecticidal (9), and peramine is a potent deterrent of feeding by insects, including the agriculturally important invertebrate pest Listronotus bonariensis (Argentine stem weevil) (10-12).Peramine synthesis is catalyzed by the two-module nonribosomal peptide synthetase (NRPS), peramine synthetase (PerA), encoded by the 8.3-kb gene perA (12). The first module of PerA contains an adenylation (A1) domain responsible for selection and activation of t...

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Section: Resultsmentioning

confidence: 99%

Disparate Independent Genetic Events Disrupt the Secondary Metabolism Gene perA in Certain Symbiotic Epichloë Species

Berry

Takach

Schardl

et al. 2015

Appl Environ Microbiol

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“…Analysis of alkaloid gene complements such as we have performed here, combined with knowledge of the associated biochemical pathways, allows estimation for the production of stable pathway intermediates and end products (Fig. S3) (Schardl et al ., , b, ). In this study, we used markers designed to test for the presence of genes associated with key alkaloid biosynthesis steps enabling prediction of the alkaloid chemotype of the B. laevipes endophytes (Tables and , Fig.…”

Section: Discussionmentioning

confidence: 99%

Interspecific hybridization and bioactive alkaloid variation increases diversity in endophyticEpichloëspecies ofBromus laevipes

Charlton

Craven

Afkhami

et al. 2014

FEMS Microbiol Ecol

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Studying geographic variation of microbial mutualists, especially variation in traits related to benefits they provide their host, is critical for understanding how these associations impact key ecological processes. In this study, we investigate the phylogenetic population structure of Epichloë species within Bromus laevipes, a native cool-season bunchgrass found predominantly in California. Phylogenetic classification supported inference of three distinct Epichloë taxa, of which one was nonhybrid and two were interspecific hybrids. Inheritance of mating-type idiomorphs revealed that at least one of the hybrid species arose from independent hybridization events. We further investigated the geographic variation of endophyte-encoded alkaloid genes, which is often associated with key benefits of natural enemy protection for the host. Marker diversity at the ergot alkaloid, loline, indole-diterpene, and peramine loci revealed four alkaloid genotypes across the three identified Epichloë species. Predicted chemotypes were tested using endophyte-infected plant material that represented each endophyte genotype, and 11 of the 13 predicted alkaloids were confirmed. This multifaceted approach combining phylogenetic, genotypic, and chemotypic analyses allowed us to reconstruct the diverse evolutionary histories of Epichloë species present within B. laevipes and highlight the complex and dynamic processes underlying these grass-endophyte symbioses.

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“…For AR3046, 43,768,368 78 bp read pairs with an insert size of ~290 bp were individually mapped to E. baconii strain ATCC 200745 and E. bromicola strain AL0434 (Schardl et al, 2014). For AR1006, 21,293,733 100 bp read pairs with an insert size of ~160 bp were mapped to E. typhina strain ATCC 200736 and E. bromicola strain AL0434.…”

Section: Methodsmentioning

confidence: 99%

cAMP Signaling Regulates Synchronised Growth of Symbiotic Epichloë Fungi with the Host Grass Lolium perenne

et al. 2016

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The seed-transmitted fungal symbiont, Epichloë festucae, colonizes grasses by infecting host tissues as they form on the shoot apical meristem (SAM) of the seedling. How this fungus accommodates the complexities of plant development to successfully colonize the leaves and inflorescences is unclear. Since adenosine 3′, 5′-cyclic monophosphate (cAMP)-dependent signaling is often essential for host colonization by fungal pathogens, we disrupted the cAMP cascade by insertional mutagenesis of the E. festucae adenylate cyclase gene (acyA). Consistent with deletions of this gene in other fungi, acyA mutants had a slow radial growth rate in culture, and hyphae were convoluted and hyper-branched suggesting that fungal apical dominance had been disrupted. Nitro blue tetrazolium (NBT) staining of hyphae showed that cAMP disruption mutants were impaired in their ability to synthesize superoxide, indicating that cAMP signaling regulates accumulation of reactive oxygen species (ROS). Despite significant defects in hyphal growth and ROS production, E. festucae ΔacyA mutants were infectious and capable of forming symbiotic associations with grasses. Plants infected with E. festucae ΔacyA were marginally less robust than the wild-type (WT), however hyphae were hyper-branched, and leaf tissues heavily colonized, indicating that the tight regulation of hyphal growth normally observed in maturing leaves requires functional cAMP signaling.

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Genomes of Plant-Associated Clavicipitaceae

Cited by 33 publications

References 90 publications

Disparate Independent Genetic Events Disrupt the Secondary Metabolism Gene perA in Certain Symbiotic Epichloë Species

Disparate Independent Genetic Events Disrupt the Secondary Metabolism Gene perA in Certain Symbiotic Epichloë Species

Interspecific hybridization and bioactive alkaloid variation increases diversity in endophyticEpichloëspecies ofBromus laevipes

cAMP Signaling Regulates Synchronised Growth of Symbiotic Epichloë Fungi with the Host Grass Lolium perenne

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